Original Research Article
The influence of exogenous methyl jasmonate on the germination and, content and composition of flavonoids in extracts from seedlings of yellow and narrow-leafed lupine

https://doi.org/10.1016/j.jfca.2019.103398Get rights and content

Highlights

  • Due to high protein and low contents of anti-nutritional substances, seeds of modern lupine CVs are used as feed additives as well as in human diets.

  • The chemical composition of modern varieties of white and narrow-leafed lupin seeds allows their use in human diets.

  • Knowing the role of jasmonates as mediators of plants' response to stress will improve lupine yielding and reduce the amount of fungicides used.

  • The use of jasmonates has a positive effect on the increase in the content of health-promoting substances in seeds.

  • Application of jasmonates causes increase of phenolic compounds in seeds, which in some cases have an anti-cancerogenic effect.

Abstract

The aim of this study was to determine the influence of exogenous methyl jasmonate (MJ) on the content and composition of flavonoids (isoflavones) in extracts from hypocotyls (with cotyledons) and radicles of yellow lupine (Lupinus luteus L.) var. Polo and in extracts from radicles of narrow-leafed lupine (Lupinus angustifolius) var. Graf. Lupine seeds were harvested when fully ripe. Two months after harvest, the effect of various MJ concentrations (10−6 M to 10-3M) on seed viability, seed vigor and the content and composition of flavonoids in extracts from seedlings that emerged from germinated lupine seeds (72 h, 20 °C) was determined. At high concentrations (10-4 M to 10-3 M), MJ suppressed the germination rate and germination capacity of seeds and decreased the growth rate of seedlings of the analyzed varieties of yellow and narrow-leafed lupines in the first 5 days of growth. In seedlings, MJ significantly increased the content of isoflavones (including daidzin, genistin, daidzein, and genistein) in 3-day-old hypocotyls (with cotyledons) and radicles of yellow lupine. This correlation was also observed in the hypocotyls (with cotyledons) and radicles of 3-day-old narrow-leafed lupine seedlings treated with MJ. Narrow-leafed lupine seeds were more sensitive to exogenous MJ then yellow lupine seeds during germination.

Introduction

The structures and biosynthetic pathways of jasmonates, mainly jasmonic acid (JA) and methyl jasmonate (MJ), are similar to those of prostaglandins found in animals. Jasmonates have various effects and are capable of inducing (microtubule decomposition, phytoalexin and alkaloid synthesis, tuber formation, shoot shortening), stimulating (aging, chlorophyll degradation, respiration, and leaf shedding) and inhibiting (Rubisco synthesis, photosynthesis, cell division, embryogenesis, flowering, and seed germination) various biological processes (Sembdner and Parthier, 1993). Exogenous MJ modifies the activity of α-D-galactosidase and the composition of carbohydrates in yellow lupine seedlings (Zalewski et al., 2010). Foliar-applied MJ changes the expression of genes encoding fruit ripening, pollen production, shoot growth, root hair growth and resistance to pathogens (Creelman and Mullet, 1997). Jasmonates play an important role in the production of secondary metabolites, including flavonoids. Mechanical injury, pest damage and fungal infections lead to the release of linolenic acid from membrane lipids. Linolenic acid is converted to JA in the octadecanoid pathway. In cells, higher concentrations of JA influence the expression of various genes involved in defense. Jasmonic acid also stimulates anthocyanin biosynthesis (Grzesiuk et al., 2008). Jasmonates resemble abscisic acid in many respects, in particular with regard to plant responses to stress (Parthier, 1991). Jasmonic acid and MJ are the key signaling compounds that induce the expression of genes encoding inhibitors of proteinases (proteins that protect plants against insects) in response to plant damage (Farmer and Ryan, 1990). Methyl jasmonate increases the transcription of genes encoding defensins (PDE 1.2) and thionins (THI 2.1), proteins with antibacterial properties (Farmer and Ryan, 1990; Szczegielniak, 2006). Jasmonic acid-dependent signaling pathways activate systemic responses, whereas JA-independent signaling pathways are involved in tissue repair and pathogen defense (Szczegielniak, 2006). According to (Fonseca et al., 2009), jasmonates regulate plant development and adaptation to adverse environmental conditions by deactivating selected natural plant hormones. When applied directly to leaves, JA increases the total phenolic content of basil plants. As an abiotic elicitor, JA could be used to enhance the biological activity and health benefits of sweet basil landraces (Malekpoor et al., 2016). The resistance of tomato seedlings to Fusarium oxysporum f. sp. lycopersici increased 4 weeks after inoculation when tomato seeds had been immersed in a solution of 0.1 mM methyl jasmonate for 1 h. At concentrations of 0.01, 0.1 and 1 mM, MJ inhibited spore germination and the growth of the fungal strain in vitro (Król et al., 2015).

The MJ-induced increase in the content of phenolic compounds in plants delivers health benefits to consumers. The positive influence of jasmonates on reducing the development of some human cancer diseases has already been proven (Majewska-Wierzbicka et al., 2012; Yach et al., 2004). Research indicates that jasmonates reduce the risk of certain cancers in humans (Majewska-Wierzbicka et al., 2012). Methyl jasmonate inhibits the proliferation of neuroma and prostate cancer cells, and it significantly decreases the risk of prostate cancer (Tong et al., 2008). Spraying friut with MJ before harvest has positive health implications for consumers (Reyes-Díaz et al., 2016). There is growing evidence to indicate that this plant hormone has health benefits for humans and animals, therefore; it will continue to be a subject of debate in the future (Cohen and Flescher, 2009; Umukoro et al., 2011). Seeds with proteins as their basic material react more strongly than oilseeds eg. sunflower seeds (Białecka and Kępczyński, 2003). This was one of the reasons for using lupine seeds in experiments. In addition, several species of lupins are cultivated in Poland, but only eleven species are grown on the production fields. Three of them are grown for fodder purposes: yellow, narrow-leaved and white lupins. The growing area is about 40,000 ha in 2017 and around 60,000 ha in 2018.

Section snippets

Materials and methods

The study was carried out on yellow and narrow-leafed lupine seedlings. Seeds were harvested when fully ripe; they were then dried and stored in linen bags at 16−18 °C and a mean humidity of 60–65%. The average thousand seed weight (at 11% moisture content) was determined to be 105.2 g for yellow lupine and 143.4 g for narrow-leafed lupine. Germination capacity was determined as the percentage of yellow lupine seeds that germinated after 21 days of imbibition and the percentage of narrow-leafed

Results

An analysis of lupine seed viability demonstrated that germination capacity exceeded 90% in both lupine species (control – germination in H2O). High concentrations of MJ (10−3 M, 10-4 M and partially 10-5 M) decreased germination rate and germination capacity. Narrow-leafed lupine seeds were more sensitive to exogenous MJ then yellow lupine seeds. An analysis of 5-day-old seedlings revealed similar results (Table 1). Methyl jasmonate exerted a more pronounced effect on yellow lupine radicles

Discussion

MJ causes less water accumulation in germinated seeds (cell wall lignification), limiting the growth of seedlings. Therefore, the content of flavonoids is presented as μg per mg of methanol extract obtained, which is common in many publications.

The observed increase in the flavonoid content of lupine seedlings treated with exogenous MJ should be analyzed from several points of view because research into flavonoids pursues several objectives. One of them is the influence of flavonoids on plant

Acknowledgements

This study was partially supported by grant No. 12.610.012-300 from the Ministry of Science and Higher Education

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